The spectrin-associated cytoskeleton in mammalian heart

Frontiers in Bioscience

Volumn 10, Issue SUPPL. 3, 2005, Pages 3020-3033

  Baines, Anthony J ^a   Pinder, Jennifer C ^b   Fordham, Jennifer ^b  

^a UNIVERSITY OF KENT   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Ankyrin; Arrhythmia; Cardiac; Cardiomyocyte; Cardiomyopathy; Cell Biology; Heart; Immunofluorescence; Intercalated Disc; Protein 4.1; Review; Sarcoplasmic Reticulum; Spectrin; T tubules; Yeast 2 Hybrid

Indexed keywords

ACTIN; ANKYRIN; ERYTHROCYTE BAND 4.1 PROTEIN; SPECTRIN;

CALCIUM TRANSPORT; CELL FUNCTION; CELL MEMBRANE; CELL TYPE; CYTOSKELETON; HEART; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILE FORCE; INTRACELLULAR MEMBRANE; MAMMAL; REVIEW; SARCOPLASMIC RETICULUM; T TUBE;

MAMMALIA;

EID: 21344469282     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1759     Document Type: Review

References (87)

1. Hiller, G. & K. Weber: Spectrin is absent in various tissue culture cells. Nature 266, 181-3. (1977)
2. Bennett, V., J. Davis & W.E. Fowler: Brain spectrin, a membrane-associated protein related in structure and function to erythrocyte spectrin. Nature 299, 126-31 (1982)
3. Glenney, J.R., Jr., P. Glenney, M. Osborn & K. Weber: An F-actin- and calmodulin-binding protein from isolated intestinal brush borders has a morphology related to spectrin. Cell 28, 843-54. (1982)
4. Goodman, S.R., I.S. Zagon & R.R. Kulikowski: Identification of a spectrin-like protein in nonerythroid cells. Proc Natl Acad Sci U S A 78, 7570-4 (1981)
5. Repasky, E.A., B.L. Granger & E. Lazarides: Widespread occurrence of avian spectrin in nonerythroid cells. Cell 29, 821-33 (1982)
6. Levine, J. & M. Willard: Fodrin: axonally transported polypeptides associated with the internal periphery of many cells. J Cell Biol 90, 631-643 (1981)
7. Bennett, V. & A.J. Baines: Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81, 1353-92. (2001)
8. Craig, S.W. & J.V. Pardo: Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to- sarcolemma attachment sites. Cell Motil 3, 449-62 (1983)
9. Nelson, W.J. & E. Lazarides: Goblin (ankyrin) in striated muscle: identification of the potential membrane receptor for erythroid spectrin in muscle cells. Proc Natl Acad Sci U S A 81, 3292-6. (1984)
10. +)ATPase and implications for the organization of membrane domains in polarized cells. Nature 328, 533-6. (1987)
11. +-ATPase, ankyrin, and fodrin in Madin-Darby canine kidney (MDCK) cells: implications for the biogenesis of epithelial cell polarity. J Cell Biol 108, 893-902. (1989)
12. Nelson, W.J., R.W. Hammerton & H. McNeill: Role of the membrane-cytoskeleton in the spatial organization of the Na,K-ATPase in polarized epithelial cells. Soc Gen Physiol Ser 46, 77-87. (1991)
13. Williams, M.W., W.G. Resneck, T. Kaysser, J.A. Ursitti, C.S. Birkenmeier, J.E. Barker & R.J. Bloch: Na,K-ATPase in skeletal muscle: two populations of beta-spectrin control localization in the sarcolemma but not partitioning between the sarcolemma and the transverse tubules. J Cell Sci 114, 751-62 (2001)
14. Mohler, P.J., J.J. Schott, A.O. Gramolini, K.W. Dilly, S. Guatimosim, W.H. DuBell, L.S. Song, K. Haurogne, F. Kyndt, M.E. Ali, T.B. Rogers, W.J. Lederer, D. Escande, H.L. Marec & V. Bennett: Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 421, 634-9 (2003)
15. Thornell, L.E., B. Johansson, A. Eriksson, V.P. Lehto & I. Virtanen: Intermediate filament and associated proteins in the human heart: an immunofluorescence study of normal and pathological hearts. Eur Heart J 5 Suppl F, 231-41 (1984)
16. Isayama, T., S.R. Goodman & I.S. Zagon: Localization of spectrin isoforms in the adult mouse heart. Cell Tissue Res 274, 127-33 (1993)
17. Flick, M.J. & S.F. Konieczny: The muscle regulatory and structural protein MLP is a cytoskeletal binding partner of betaI-spectrin. J Cell Sci 113 (Pt 9), 1553-64 (2000)
18. Kostin, S., D. Scholz, T. Shimada, Y. Maeno, H. Mollnau, S. Hein & J. Schaper: The internal and external protein scaffold of the T-tubular system in cardiomyocytes. Cell Tissue Res 294, 449-60 (1998)
19. Baklouti, F., S.C. Huang, T.J. Vulliamy, J. Delaunay & E.J. Benz, Jr.: Organization of the human protein 4.1 genomic locus: new insights into the tissue-specific alternative splicing of the pre-mRNA. Genomics 39, 289-302 (1997)
20. Kontrogianni-Konstantopoulos, A., S.C. Huang & E.J. Benz, Jr.: A nonerythroid isoform of protein 4.1R interacts with components of the contractile apparatus in skeletal myofibers. Mol Biol Cell 11, 3805-17. (2000)
21. Pasternack, G.R. & R.H. Racusen: Erythrocyte protein 4.1 binds and regulates myosin. Proc Natl Acad Sci U S A 86, 9712-6. (1989)
22. Yamakawa, H. & O. Ohara: Comparison of mRNA and protein levels of four members of the protein 4.1 family: The type II brain 4.1/4.1B/KIAA0987 is the most predominant member of the protein 4.1 family in rat brain. Gene 248, 137-145 (2000)
23. Xu, J., D. Ziemnicka, J. Scalia & L. Kotula: Monoclonal antibodies to alphaI spectrin Src homology 3 domain associate with macropinocytic vesicles in nonerythroid cells. Brain Res 898, 171-7 (2001)
24. Bennett, P.M., A.J. Baines, M.C. Lecomte, A.M. Maggs & J.C. Pinder: Not just a plasma membrane protein: in cardiac muscle cells alpha-II spectrin also shows a close association with myofibrils. J Muscle Res Cell Motil 25, 119-26. (2004)
25. Porter, G.A., M.G. Scher, W.G. Resneck, N.C. Porter, V.M. Fowler & R.J. Bloch: Two populations of beta-spectrin in rat skeletal muscle. Cell Motil Cytoskeleton 37, 7-19 (1997)
26. Baines, A.J.: Comprehensive analysis of all triple helical repeats in beta-spectrins reveals patterns of selective evolutionary conservation. Cell Mol Biol Lett 8, 195-214 (2003)
27. Pomies, P., H.A. Louis & M.C. Beckerle: CRP1, a LIM domain protein implicated in muscle differentiation, interacts with alpha-actinin. J Cell Biol 139, 157-68. (1997)
28. Hayes, N.V., C. Scott, E. Heerkens, V. Ohanian, A.M. Maggs, J.C. Pinder, E. Kordeli & A.J. Baines: Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities. J Cell Sci 113, 2023-34. (2000)
29. Hu, R.J., M. Watanabe & V. Bennett: Characterization of human brain cDNA encoding the general isoform of beta-spectrin. J Biol Chem 267, 18715-22 (1992)
30. Ma, Y., W.E. Zimmer, B.M. Riederer, M.L. Bloom, J.E. Barker, S.R. Goodman & S.M. Goodman: The complete amino acid sequence for brain beta spectrin (beta fodrin): relationship to globin sequences. Brain Res Mol Brain Res 18, 87-99. (1993)
31. Mohler, P.J., W. Yoon & V. Bennett: Ankyrin-B targets beta 2-spectrin to an intracellular compartment in neonatal cardiomyocytes. J Biol Chem 279, 40185-93 (2004)
32. Williams, M.W. & R.J. Bloch: Differential distribution of dystrophin and beta-spectrin at the sarcolemma of fast twitch skeletal muscle fibers. J Muscle Res Cell Motil 20, 383-93 (1999)
33. An, X., M.C. Lecomte, J.A. Chasis, N. Mohandas & W. Gratzer: Shear-response of the spectrin dimer-tetramer equilibrium in the red blood cell membrane. J Biol Chem 277, 31796-800 (2002)
34. Kennedy, S.P., S.A. Weed, B.G. Forget & J.S. Morrow: A partial structural repeat forms the heterodimer self-association site of all beta-spectrins. J Biol Chem 269, 11400-8 (1994)
35. Bignone, P.A. & A.J. Baines: Spectrin alpha II and beta II isoforms interact with high affinity at the tetramerization site. Biochem J 374, 613-24 (2003)
36. Taylor-Harris, P.M., L.A. Keating, A.M. Maggs, G.W. Phillips, E.J. Birks, R.C.G. Franklin, M.H. Yacoub, A.J. Baines & J.C. Pinder: Cardiac muscle cell cytoskeletal Protein 4.1: Analysis of transcripts and subcellular location - relevance to membrane integrity, microstructure and possible role in heart failure. Mammalian Genome 16, 137-151 (2005)
37. Conboy, J.: The role of alternative pre-mRNA splicing in regulating the structure and function of skeletal protein 4.1. Proc Soc Exp Biol Med 220, 73-8 (1999)
38. Gimm, J.A., X. An, W. Nunomura & N. Mohandas: Functional characterization of spectrin-actin-binding domains in 4.1 family of proteins. Biochemistry 41, 7275-82 (2002)
39. Mohler, P.J., A.O. Gramolini & V. Bennett: The ankyrin-B C-terminal domain determines activity of ankyrin-B/G chimeras in rescue of abnormal inositol 1,4,5-trisphosphate and ryanodine receptor distribution in ankyrin-B (-/-) neonatal cardiomyocytes. J Biol Chem 277, 10599-607 (2002)
40. Mohler, P.J., I. Splawski, C. Napolitano, G. Bottelli, L. Sharpe, K. Timothy, S.G. Priori, M.T. Keating & V. Bennett: A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc Natl Acad Sci U S A 101, 9137-42 (2004)
41. Mohler, P.J., J.Q. Davis, L.H. Davis, J.A. Hoffman, P. Michaely & V. Bennett: Inositol 1,4,5-trisphosphate receptor localization and stability in neonatal cardiomyocytes requires interaction with ankyrin-B. J Biol Chem 279, 12980-7 (2004)
42. 2+-ATPases, PMCA and SERCA. Manuscript submitted (2005)
43. Maximov, A., T.S. Tang & I. Bezprozvanny: Association of the type 1 inositol (1,4,5)-trisphosphate receptor with 4.1N protein in neurons. Mol Cell Neurosci 22, 271-83 (2003)
44. Zhang, S., A. Mizutani, C. Hisatsune, T. Higo, H. Bannai, T. Nakayama, M. Hattori & K. Mikoshiba: Protein 4.1N is required for translocation of inositol 1,4,5-trisphosphate receptor type 1 to the basolateral membrane domain in polarized Madin-Darby canine kidney cells. J Biol Chem 278, 4048-56 (2003)
45. Fukatsu, K., H. Bannai, S. Zhang, H. Nakamura, T. Inoue & K. Mikoshiba: Lateral diffusion of inositol 1,4,5-trisphosphate receptor type 1 is regulated by actin filaments and 4.1N in neuronal dendrites. J Biol Chem 279, 48976-82. (2004)
46. Kijima, Y., A. Saito, T.L. Jetton, M.A. Magnuson & S. Fleischer: Different intracellular localization of inositol 1,4,5-trisphosphate and ryanodine receptors in cardiomyocytes. J Biol Chem 268, 3499-506. (1993)
47. Kaysser, T.M., N.J. Wandersee, R.T. Bronson & J.E. Barker: Thrombosis and secondary hemochromatosis play major roles in the pathogenesis of jaundiced and spherocytic mice, murine models for hereditary spherocytosis. Blood 90, 4610-9 (1997)
48. Tang, Y., V. Katuri, A. Dillner, B. Mishra, C.X. Deng & L. Mishra: Disruption of transforming growth factor-beta signaling in ELF beta-spectrin-deficient mice. Science 299, 574-7 (2003)
49. Shi, Z.T., V. Afzal, B. Coller, D. Patel, J.A. Chasis, M. Parra, G. Lee, C. Paszty, M. Stevens, L. Walensky, L.L. Peters, N. Mohandas, E. Rubin & J.G. Conboy: Protein 4.1R-deficient mice are viable but have erythroid membrane skeleton abnormalities. J Clin Invest 103, 331-40. (1999)
50. Moon, R.T. & E. Lazarides: Biogenesis of the avian erythroid membrane skeleton: receptor-mediated assembly and stabilization of ankyrin (goblin) and spectrin. J Cell Biol 98, 1899-904. (1984)
51. Moon, R.T. & E. Lazarides: beta-Spectrin limits alpha-spectrin assembly on membranes following synthesis in a chicken erythroid cell lysate. Nature 305, 62-5. (1983)
52. Staufenbiel, M. & E. Lazarides: Assembly of protein 4.1 during chicken erythroid differentiation. J Cell Biol 102, 1157-63. (1986)
53. Agre, P., E.P. Orringer & V. Bennett: Deficient red-cell spectrin in severe, recessively inherited spherocytosis. N Engl J Med 306, 1155-61 (1982)
54. Mohandas, N., W.M. Phillips & M. Bessis: Red blood cell deformability and hemolytic anemias. Semin Hematol 16, 95-114 (1979)
55. Olson, E.N.: A decade of discoveries in cardiac biology. Nat Med 10, 467-74 (2004)
56. Maron, B.J., J.M. Gardin, J.M. Flack, S.S. Gidding, T.T. Kurosaki & D.E. Bild: Prevalence of hypertrophic cardiomyopathy in a general population of young adults. Echocardiographic analysis of 4111 subjects in the CARDIA Study. Coronary Artery Risk Development in (Young) Adults. Circulation 92, 785-9 (1995)
57. Elliott, P. & P.W.J. McKenna: Hypertrophic cardiomyopathy. The Lancet 363, 1881-1891 (2004)
58. Shaw, T., P. Elliott & W.J. McKenna: Dilated cardiomyopathy: a genetically heterogeneous disease. The Lancet 360, 654-655 (2002)
59. Crilley, J.G., E.A. Boehm, E. Blair, B. Rajagopalan, A.M. Blamire, P. Styles, W.J. McKenna, I. Ostman-Smith, K. Clarke & H. Watkins: Hypertrophic cardiomyopathy due to sarcomeric gene mutations is characterized by impaired energy metabolism irrespective of the degree of hypertrophy. J Am Coll Cardiol 41, 1776-82 (2003)
60. Watkins, H.: Genetic clues to disease pathways in hypertrophic and dilated cardiomyopathies. Circulation 107, 1344-6 (2003)
61. Mishra, L., T. Cai, P. Yu, S.P. Monga & B. Mishra: Elf3 encodes a novel 200-kD beta-spectrin: role in liver development. Oncogene 18, 353-64 (1999)
62. Arber, S., J.J. Hunter, J. Ross, Jr., M. Hongo, G. Sansig, J. Borg, J.C. Perriard, K.R. Chien & P. Caroni: MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88, 393-403 (1997)
63. Ehler, E., R. Horowits, C. Zuppinger, R.L. Price, E. Perriard, M. Leu, P. Caroni, M. Sussman, H.M. Eppenberger & J.C. Perriard: Alterations at the intercalated disk associated with the absence of muscle LIM protein. J Cell Biol 153, 763-72 (2001)
64. Messina, D.N., M.C. Speer, M.A. Pericak-Vance & E.M. McNally: Linkage of familial dilated cardiomyopathy with conduction defect and muscular dystrophy to chromosome 6q23. Am J Hum Genet 61, 909-17 (1997)
65. Erdel, M., H.C. Duba, I. Verdorfer, A. Lingenhel, R. Geiger, K.H. Gutenberger, E. Ludescher, B. Utermann & G. Utermann: Comparative genomic hybridization reveals a partial de novo trisomy 6q23-qter in an infant with congenital malformations: delineation of the phenotype. Hum Genet 99, 596-601 (1997)
66. Thierfelder, L.: Genetics of dilated cardiomyopathy (Article in German). Med Klin (Munich) 93, 210-4 (1998)
67. Schonberger, J., H. Levy, E. Grunig, S. Sangwatanaroj, D. Fatkin, C. MacRae, H. Stacker, C. Halpin, R. Eavey, E.F. Philbin, H. Katus, J.G. Seidman & C.E. Seidman: Dilated Cardiomyopathy and Sensorineural Hearing Loss : A Heritable Syndrome That Maps to 6q23-24. Circulation 101, 1812-1818 (2000)
68. Edwards, Y.H. & D.M. Swallow: Mutation and Protein Dysfunction. In: Protein dysfunction in human genetic disease Eds: D.M. Swallow and Y.H. Edwards, Bios Scientific Publishers, London, UK (1997). (1997)
69. Palek, J. & S.E. Lux: Red cell membrane skeletal defects in hereditary and acquired hemolytic anemias. Semin Hematol 20, 189-224 (1983)
70. Tse, W.T. & S.E. Lux: Red blood cell membrane disorders. Br J Haematol 104, 2-13 (1999)
71. Gascard, P. & N. Mohandas: New insights into functions of erythroid proteins in nonerythroid cells. Curr Opin Hematol 7, 123-9 (2000)
72. Speicher, D.W.: The present status of erythrocyte spectrin structure: the 106-residue repetitive structure is a basic feature of an entire class of proteins. J Cell Biochem 30, 245-58 (1986)
73. Morita, M., M. Hashizume, T. Kanematsu, K. Sugimachi & K. Makizumi: Hereditary spherocytosis with congestive heart failure: report of a case. Surg Today 23, 458-61. (1993)
74. Moiseyev, V.S., E.A. Korovina, E.L. Polotskaya, I.S. Poliyanskaya & V.V. Yazdovsky: Hypertrophic cardiomyopathy associated with hereditary spherocytosis in three generations of one family. Lancet 2, 853-4. (1987)
75. Pinder, J.C. & A.J. Baines: A protein accumulator. Nature 406, 253-4. (2000)
76. Mohler, P.J., I. Rivolta, C. Napolitano, G. Lemaillet, S. Lambert, S.G. Priori & V. Bennett: Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc Natl Acad Sci U S A 101, 17533-8. (2004)
77. Durand, J.-B., L.L. Bachinski, L.C. Bieling, G.Z. Czernuszewicz, A.B. Abchee, Q. Tao Yu, T. Tapscott, R. Hill, J. Ifegwu, A.J. Marian, R. Brugada, S. Daiger, J.M. Gregoritch, J.L. Anderson, M. Quinones, J.A. Towbin & R. Roberts: Localization of a Gene Responsible for Familial Dilated Cardiomyopathy to Chromosome 1q32. Circulation 92, 3387-3389 (1995)
78. Christiansen, J., J.D. Dyck, B.G. Elyas, M. Lilley, J.S. Bamforth, M. Hicks, K.A. Sprysak, R. Tomaszewski, S.M. Haase, L.M. Vicen-Wyhony & M.J. Somerville: Chromosome 1q21.1 Contiguous Gene Deletion Is Associated With Congenital Heart Disease. Circ Res 94, 1429-1435 (2004)
79. Pasotti, M., A. Repetto, A. Pisani & E. Arbustini: Diseases associated with lamin A/C gene defects: what the clinical cardiologist ought to know (Article in Italian). Ital Heart J Suppl 5, 98-111 (2004)
80. Debrus, S., A. de Meeus, M.K. Jean & P. Bouvagnet: Genetics of hereditary cardiopathies; (Article in French). Arch Mal Coeur Vaiss 89, 619-27 (1996)
81. Nava, A., B. Bauce, C. Basso, M. Muriago, A. Rampazzo, C. Villanova, L. Daliento, G. Buja, D. Corrado, G.A. Danieli & G. Thiene: Clinical profile and long-term follow-up of 37 families with arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol 36, 2226-33 (2000)
82. Frances, R., A.M. Rodriguez Benitez & D.R. Cohen: Arrhythmogenic right ventricular dysplasia and anterior polar cataract. Am J Med Genet 73, 125-6 (1997)
83. Rampazzo, A., A. Nava, G.A. Danieli, G. Buja, L. Daliento, G. Fasoli, R. Scognamiglio, D. Corrado & G. Thiene: The gene for arrhythmogenic right ventricular cardiomyopathy maps to chromosome 14q23-q24. Hum Mol Genet 3, 959-62 (1994)
84. Wilcox, M.A., D.F. Wyszynski, C.I. Panhuysen, Q. Ma, A. Yip, J. Farrell & L.A. Farrer: Empirically derived phenotypic subgroups - qualitative and quantitative trait analyses. BMC Genet 1:, S15 (2003)
85. DeStefano, A.L., G.A. Gates, N. Heard-Costa, R.H. Myers & C.T. Baldwin: Genomewide linkage analysis to presbycusis in the Framingham Heart Study. Arch Otolaryngol Head Neck Surg Mar; 129, 285-9. (2003)
86. Luo, K., W. Yuan, C. Zhu, Y. Li, Y. Wang, W. Zeng, W. Jiao, M. Liu & X. Wu: Expression of a novel Krupple-like zinc-finger gene, ZNF382, in human heart. Biochemical and Biophysical Research Communications 299, 606-612 (2002)
87. Wilcken, D.E.: Overview of inherited metabolic disorders causing cardiovascular disease. J Inherit Metab Dis 26, 245-57 (2003)